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Effect of Membrane Environment on the Ligand-Binding Properties of the Terminal Oxidase Cytochrome bd-I from Escherichia coli

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Abstract

Cytochrome bd-I is a terminal oxidase of the Escherichia coli respiratory chain. This integral membrane protein contains three redox-active prosthetic groups (hemes b558, b595, and d) and couples the electron transfer from quinol to molecular oxygen to the generation of proton motive force, as one of its important physiological functions. The study was aimed at examining the effect of the membrane environment on the ligand-binding properties of cytochrome bd-I by absorption spectroscopy. The membrane environment was found to modulate the ligand-binding characteristics of the hemoprotein in both oxidized and reduced states. Absorption changes upon the addition of exogenous ligands, such as cyanide or carbon monoxide (CO), to the detergent-solubilized enzyme were much more significant and heterogeneous than those observed with the membrane-bound enzyme. In the native membranes, both cyanide and CO interacted mainly with heme d. An additional ligand-binding site (heme b558) appeared in the isolated enzyme, as was evidenced by more pronounced changes in the absorption in the Soret band. This additional reactivity could also be detected after treatment of E. coli membranes with a detergent. The observed effect did not result from the enzyme denaturation, since reconstitution of the isolated enzyme into azolectin liposomes restored the ligand-binding pattern close to that observed for the intact membranes.

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Abbreviations

BQCl4 :

tetrachloro-1,4-benzoquinone

Ches:

2-(cyclohexylamino)ethanesulfonic acid

CO:

carbon monoxide

cryo-EM:

single-particle cryo-electron microscopy

E m :

midpoint redox potential

Hepes:

N-(2-Hydroxyethyl)piperazine-N-2-ethanesulfonic acid

SB-12:

dodecyl-N,N-dimethyl-ammonio-3-propane-sulfonate

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Acknowledgements

The author thanks V. P. Skulachev for his interest in this work and useful discussion, I. A. Smirnova for her help in the initial stage of the experiments and valuable suggestions, and R. B. Gennis for kindly provided E. coli strain GO105/pTK1. The author would also like to express his deepest gratitude to A. A. Konstantinov (passed away 1st May, 2020), who had inspired the author to perform this work.

Funding

This work was supported by the Russian Science Foundation (project no. 19-14-00063).

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  1. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    V. B. Borisov

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Borisov, V.B. Effect of Membrane Environment on the Ligand-Binding Properties of the Terminal Oxidase Cytochrome bd-I from Escherichia coli. Biochemistry Moscow 85, 1603–1612 (2020). https://doi.org/10.1134/S0006297920120123

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